Theta Oscillations In Human Memory

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Trends in Cognitive SciencesFeature ReviewTheta Oscillations in Human MemoryNora A. Herweg,1,2 Ethan A. Solomon,1,2 and Michael J. Kahana1,*Theta frequency (4–8 Hz) fluctuations of the local field potential have long beenimplicated in learning and memory. Human studies of episodic memory,however, have provided mixed evidence for theta’s role in successful learningand remembering. Re-evaluating these conflicting findings leads us to concludethat: (i) successful memory is associated both with increased narrow-band thetaoscillations and a broad-band tilt of the power spectrum; (ii) theta oscillationsspecifically support associative memory, whereas the spectral tilt reflects a general index of activation; and (iii) different cognitive contrasts (generalized versusspecific to memory), recording techniques (invasive versus noninvasive), andreferencing schemes (local versus global) alter the balance between the twophenomena to make one or the other more easily detectable.HighlightsInfluential theories state that human declarative memory relies on the same neural machinery as spatial navigation andspecifically implicate the theta rhythm inmemory formation for associations between sequentially visited places and experiences events.Electrophysiological studies in humans,however, paint a complicated picture oftheta’s role in episodic memory.Whereas some studies observe increases in theta power associatedwith successful memory, other studiesobserve a spectral tilt of the powerspectrum with increased high frequencyand decreased low-frequency powerduring successful memory formation orretrieval.The Theta HypothesisForming associations between different aspects of our sensory and cognitive experience allowsus to remember specific events and abstract knowledge about the world that surrounds us.Our coworkers do not query us each morning about who we are and where we are from, sincethey have associated that information with the visual inputs corresponding to our faces. If they instead ask us how our weekend was, we can use that cue to remember our visit to the beach andtell them about our experience. We do not need to consult a map to make it from our desks to thecoffee machine, since we have associated those objects with locations in space. And we also donot need to worry about our coffee being too hot, since we have associated the machine’s outputwith a reasonable temperature. It could have been a very bewildering and inefficient start to ourday, but thanks to associations, it was not.Here, we reconcile these findings byconsidering the distinction betweennarrow-band theta oscillations and cooccurring broad-band effects. We showhow recording methods as well as analytical choices may alter the balance between the two phenomena.The neural machinery responsible for the formation of associations between high-dimensionalrepresentations resides primarily in the medial temporal lobe (MTL), containing the hippocampus,entorhinal, perirhinal, and parahippocampal cortices. Communication and processing withinthese regions, and between these regions and neocortical association areas, has been linkedto episodic memory (see Glossary) [1] and spatial navigation [2,3], Both navigating and remembering involve associations either between the sensory and cognitive components that comprisean event, or between the features that mark specific locations in space. And potentially key tothese functions is a physiological signature called the theta rhythm: a 4–8 Hz oscillation in thelocal field potential (LFP) that was first characterized in rodents in the 1930s (Box 1).In subsequent decades, a vast theoretical and empirical enterprise has grown around the thetarhythm. Theta appears in several mammalian species, including humans, and is most commonlyobserved during active exploration. Theta phase has been linked to the firing of MTL neurons thatrepresent specific locations in space. The finding that hippocampal place cells fire at progressively earlier phases of the theta rhythm as an animal traverses a cell’s firing field [4] inspired apowerful conceptualization of MTL function [5]. In this framework, the ongoing theta rhythmforms a consistent reference for distributed cellular activity, allowing for coding of informationnot only in firing rates but also in spike-phase relations. Furthermore, the systematic coactivationof sequentially visited places allows for spike-timing dependent plasticity (STDP) to208Trends in Cognitive Sciences, March 2020, Vol. 24, No. 3 2019 Elsevier Ltd. All rights 61Department of Psychology, Universityof Pennsylvania, Philadelphia, PA, USA2These authors contributed equally tothis work*Correspondence:[email protected](M.J. Kahana).

Trends in Cognitive SciencesBox 1. Theta Oscillations Associated with Movement and CognitionTheta oscillations were first discovered in the rabbit hippocampus in 1938 [83], where they were found to occur both spontaneously and as a reaction to painful stimuli. A first link to memory was established when researchers followed up this discovery by showing that the duration of cortical theta oscillations recorded in rats after an aversive foot shock correlates withlater memory for that foot shock [84]. Even though many early studies in rodents were mainly focused on theta’s role involuntary movement, where theta oscillations can be observed reliably and with large amplitudes [85,86], some studieshave noted that theta oscillations also occur during immobility [87]. The theta-memory link was later specifically strengthened by studies showing that the phase of theta oscillations modulates synaptic plasticity [88–90].Whereas early studies failed to identify a clear homologue of rodent theta in the human brain [91,92], later studies identifiedtask-dependent theta oscillations during virtual navigation [8], and showed that these oscillations occur in shorter episodes[58,93] and with a lower frequency compared with the movement-related theta in rodents [94,95]. In humans, as in rodents, theta oscillations appear prominently during movement [2], but they can also be observed in a variety of cognitivetasks [96]. In addition to theta’s proposed role in declarative memory (Box 2), theta oscillations may support working memory [97–100] and cognitive control [101], as well as rhythmic shifts of spatial attention [102].strengthen associations between sequentially activated cells with a bias for forward-associations(Box 2 and Figure 1). This mechanism does not have to be specific to spatial memory but may beimportant for establishing temporal associations between arbitrary stimuli. And indeed, it can berelated to two hallmark findings of episodic free recall: temporal contiguity, the tendency to successively remember items experienced in temporal proximity; and forward-asymmetry, a bias forforward-transitions [6]. In essence, the stream of sensory inputs to the brain is compressed by thetheta rhythm, allowing MTL circuitry to form associations between sequential inputs. Over timeand repeated encounters of the same stimuli in different sequences, this mechanism may leadto the formation of ‘cognitive maps’ that reflect long-standing associations between all kinds ofstimuli (such as places or concepts; Box 2) [5,7].But if the theta rhythm truly supports effective encoding of episodic associations, it is surprisingthat the brain does not always show it. Whereas electrophysiological studies in humans havereplicated increases in MTL and hippocampal theta power during spatial navigation [8–12],recordings during the formation of episodic memories have revealed an inconsistent relationshipbetween theta and successful memory encoding. In some experiments, increases in MTL andBox 2. Mechanistic Accounts of Theta’s Role in MemoryTheorists have proposed several mechanistic accounts for theta’s role in memory. Here we consider two such accounts:(i) the separate phases of encoding and retrieval (SPEAR) model of Hasselmo and colleagues [103,104], and (ii) the temporal encoding model of Buzsáki [5].The SPEAR model posits that different phases of the theta rhythm are associated with a bias of the CA1 region of the hippocampus to preferentially process input from the entorhinal cortex or from area CA3. This bias, along with phasicchanges in long-term potentiation (LTP) and depression (LTD), is thought to separate encoding (entorhinal cortex, LTP)and retrieval (CA3, LTD) processes in the hippocampal circuit to the peak and the trough of theta, respectively. The modelis consistent with theta phase reset in response to behaviorally relevant stimuli [39,105], as well as with theta phase precession of place cells [4,39]. In this framework, phase precession arises from retrieved/anticipated activity and stimulusdriven activity that occur at different theta phases.Buzsáki’s temporal encoding model sees theta as critical for establishing temporal associations between stimuli [5,106].Phase precession of place cells produces a time-compressed sequence of firing representing sequentially visited placeswithin each theta cycle (Figure 1). Due to this temporal compression, cells fire at delays short enough to enable STDP tostrengthen associations between sequentially visited places, preferentially in the forward direction. This mechanism maybe at play during navigation, as well as when experiencing sequences of arbitrary stimuli, such as words in a free-recalltask. It would thereby explain subjects’ tendency to successively recall items experienced in succession (temporal contiguity effects) and in the forward direction (asymmetry effect) [6]. Experiencing the same places or items in different sequential order would ultimately lead to the generation of spatial or semantic maps, which reflect the long-standing temporal cooccurrence of places or concepts.GlossaryBroad-band effect: using Fouriertransform or related methods, thepotentials measured with EEG can bedecomposed into their constituentfrequencies. The resulting powerspectrum exhibits a 1/f shape withhigher power at lower frequencies;changes in slope and offset of thisbackground spectrum are referred to asbroad-band effects or, more specifically,as ‘tilt’ and ‘shift’. These should bedistinguished from narrow-bandoscillations, which can be detected as apeak in the power spectrum thatdeviates from the 1/f backgroundspectrum.Electroencephalography (EEG):method to record electrical potentialsgenerated by neuronal activity usingelectrodes placed on the scalp (scalpEEG), on the cortical surface (ECoG), orwithin the brain (depth electrodes orstereo EEG); The latter two are jointlyreferred to as intracranial EEG (iEEG).Episodic memory: memory forpersonally experienced events that areassociated with a particular time andspace.Local field potential (LFP): electricalpotential generated by changes in ionconcentrations as a result of neuronalactivity. LFPs can be recorded byplacing electrodes in the extracellularspace.Magnetoencephalography (MEG):method to record electromagnetic fieldsgenerated by neuronal activity withsensors surrounding the head.Oscillation: rhythmic fluctuation of theLFP at a particular frequency. At eachtime point, oscillations can becharacterized by instantaneousamplitude and phase of the oscillation. Inthe frequency domain, oscillationsshould be detectable as a peak relativeto the background power spectrum.Phase synchronization: constantphase offset across trials or time-pointsbetween oscillations at differentrecording electrodes.Place cells: neurons in the medialtemporal lobe that fire when an animal islocated in a particular location in space:the cell’s place field.Recall Task: memory task in whichsubjects encode lists of items (e.g.,words) and subsequently recall thoseitems. In ‘free recall’ subjects recall theitems in any order they come to mind.In ‘cued recall’ subjects encode pairsof items, so that during recall one ofTrends in Cognitive Sciences, March 2020, Vol. 24, No. 3209

Trends in Cognitive Sciencesneocortical theta power are predictive of good episodic memory. But over a dozen recent studieshave shown exactly the opposite: widespread decreases in theta power during successfulepisodic encoding and retrieval. These findings undercut the idea that the theta rhythm is ageneral-purpose mechanism that links episodic memory and spatial navigation under the umbrella of cognitive mapping. If the MTL is agnostic to the type of information it is acting upon,why should theta power increase during spatial navigation but decrease during the formation ofevent memories?Here, we seek to reconcile the conflicting literature regarding theta’s role in human episodic memory. First, we will review electrophysiological studies that report increases, decreases, or mixedeffects of theta activity during episodic memory tasks. In doing so, we will address how the recording methods, as well as particular experimental and analytical methods, may be responsiblefor reported increases or decreases in theta power during successful memory encoding and retrieval. We specifically highlight how contrasts that compare activity for remembered and forgotten stimuli, though commonly used in the literature, inherently confound associational memoryprocesses with a diverse array of other cognitive functions that support successful task completion. These confounds make it difficult to interpret the results and are a key factor behind the conflicting findings. To that end, we will offer a defense for the prevailing theta hypothesis, explaininghow the existing body of literature in spatial and episodic domains supports the idea that the thetarhythm underlies associative processing in the brain.Electrophysiological Studies of the Theta Rhythm in HumansThe oscillatory correlates of human memory have been intensively studied for over 25 years usingboth noninvasive [scalp electroencephalography (EEG) and magnetoencephalography(MEG)] and invasive [intracranial EEG (iEEG) or electrocorticography (ECoG)] recordingtechniques (see Box 3 for a discussion on the origin of theta effects observed with both kindsthe items serves as a cue and theother one has to be recalled.Recognition Task: memory task inwhich subjects encode lists of items andsubsequently judge whether each of aseries of test items was or was notpresent on the studied list.Reference: EEG records potentialsbetween pairs of electrodes.During recording, all electrodes arecommonly paired with a singlereference electrode. For offlineanalysis, data can be re-referenced;this can, for instance, be done bysubtracting from each electrodes’time series the time series of itsclosest neighboring electrode(i.e., bipolar referencing scheme) orthe average time series of allelectrodes (i.e., average referencingscheme).Spike-timing dependent plasticity(STDP): process by which thestrength of synaptic connectionsbetween neurons are strengthened orweakened based on the relative timingof action potentials (spikes) of theneurons. If a neuron tends to receive acertain input before it spikes, thatconnection will be strengthened; if ittends to receive a certain input after itspikes, that connection will beweakened.Trends in Cognitive SciencesFigure 1. Formation of Associative Memories via Theta Oscillations. (A) Spatial navigation constitutes a sequential set of sensory inputs that correspond tolocations in space. Neural representations of a location become stronger the closer the observer is to that location. Locations exist as two (or three) dimensionalcoordinates. (B) Episodic memory, such as learning a list of nouns, consists of a sequential set of inputs that correspond to semantic and temporal features ofencountered words. Words exist as locations in a multidimensional semantic/temporal feature space. (C) Theta oscillations serve to organize sequential inputs, byrepresenting multiple locations or items within a single theta cycle [5]. The current location or item is represented most strongly, but prior and forthcomingrepresentations are also activated, though to a lesser degree. See Box 2 for further details. Panel (C) adapted from [2].210Trends in Cognitive Sciences, March 2020, Vol. 24, No. 3

Trends in Cognitive SciencesBox 3. Theta Oscillations: A Phenomenon of the Hippocampus, Neocortex, or Both?A wealth of recording methods have yielded a complicated picture of where theta is fundamentally generated. The originalresearch focus on LFP recordings of hippocampal theta in rodents led to the discovery of a circuit that generates 3–8 Hzoscillations, centered on the MTL [107]. Volume conduction and projections from the MTL to neocortical areas could serveto entrain other brain regions to that MTL-derived rhythm, explaining how electrodes placed at the cortical surface (ECoG)or scalp (EEG) can detect theta rhythms during cognitive tasks [9]. However, subsequent research identified independentgenerators of the theta rhythm in the neocortex itself [108,109], which could more directly contribute to theta power detected by ECoG or scalp sensors. It is not known to what extent theta detected at the scalp or cortical surface reflect hippocampal versus neocortically generated rhythms, though this is a key question in human electrophysiology.In humans, simultaneous recording of cortical surface and MTL potentials via ECoG and depth electrodes, respectively,tend to demonstrate broadly similar patterns of electrical activity during cognition. As noted in this review (Figure 2), intracranial SMEs tend to show decreases in theta power and increases in high-frequency activity at both the cortical surfaceand in hippocampus/MTL [46,49]. A high-powered study of spectral power in hippocampal subfields showed remarkablyconsistent SMEs with prior studies of ECoG potentials [46]. Furthermore, a broad set of neocortical areas become phasesynchronized with each other and with the MTL during successful memory formation and retrieval [51,110]. Another studyfound that electrical stimulation in the MTL could evoke oscillatory events in functionally connected neocortical regions[111]. However, it remains unclear whether this synchronization is due to direct entrainment of the cortex by the hippocampus or induced synchronization between two independently generated rhythms.In this review, we address a wide range of literature that considers electrical potentials derived from scalp EEG, MEG, iEEGdepth electrodes, and ECoG. We directly discuss the differences between scalp EEG and intracranial recordings at thecortical surface (see ‘Why the scalp/invasive discrepancy?’). Establishing exactly how neocortical and hippocampal thetarhythms interact and differentially contribute to episodic memory is an important question for future study.of methods). These studies have shown variable evidence for theta oscillations during humanepisodic memory; some studies report memory-related theta increases while othersreport decreases. In many cases memory-related theta increases and decreases werefound in the same study, depending on when and where in the brain oscillatory powerwas examined.Beyond recording methods, studies of human theta activity also differ in their analysis schemes.During encoding, studies commonly compare patterns of spectral power between items thatwere subsequently remembered versus not-remembered [the ‘subsequent memory effect’(SME)]. During retrieval, studies compare activity surrounding the presentation of a cue or, infree recall, they compare correct recalls with time periods where no recall occurs. Suchmemory-success analyses may obscure neural dynamics that differentially support differentkinds of successful memory encoding or retrieval. Therefore, the second most common approach is to assess the correlation between neural activity and a specific measure of associativememory formation. For example, one study [13] contrasted activity relating to the accuracy ofspatial recalls, while another study [14] contrasted activity relating to the recall of spatially proximate versus spatially dist

Apr 11, 2018 · Theta Oscillations in Human Memory Nora A. Herweg,1,2 Ethan A. Solomon,1,2 and Michael J. Kahana1,* Theta frequency (4–8 Hz) fluctuations of the local field potential have long been implicated in learning and memory. Human studies of episodic memory, however, have provided mixed